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CAB Reviews 2021 16, No. 013

Biological control of ( gregaria Forskål)

Eunice W. Githae* and Erick K. Kuria

Address: Department of Biological Sciences, Chuka University, P.O. Box 109-60400, Chuka, .

*Correspondence: Eunice W. Githae. Email: [email protected], [email protected]

Received: 03 September 2020 Accepted: 05 January 2021 doi: 10.1079/PAVSNNR202116013

The electronic version of this article is the definitive one. It is located here:http://www.cabi.org/cabreviews

© CAB International 2021 (Online ISSN 1749-8848)

Abstract

Desert locust (Schistocerca gregaria Forskål) is one of the most serious agricultural pests in the world due to its voracity, speed of reproduction, and range of flight. We discuss the current state of knowledge on its biological control using and botanical extracts. flavoviride was among the first to be recognized as a bio-control agent against in the laboratory and field conditions. Nevertheless, its oil formulation adversely affected non- target organisms, hence led to further research on other microorganisms. var. acridum (syn. ) is an environmentally safer bio- that has no measurable impact on non-target organisms. However, there are various shortcomings associated with its use in desert locust control as highlighted in this review. Bacterial pathogens studied were from of Bacillus, Pseudomonas, and Serratia. Botanical extracts of 27 plant species were tested against the locust but showed varied results. and Melia volkensii were the most studied plant species, both belonging to family Meliaceae, which is known to have biologically active limonoids. Out of the 20 plant families identified, Apiaceae was the most represented with a frequency of 21%. However, only crude botanical extracts were used and therefore, the active ingredients against desert locust were not identified. Through a comprehensive research, an integrated management strategy that incorporates these bio-controls would be a realistic option to control desert locust infestations.

Keywords: bio-control, bio-, desert locust, microorganisms, botanical extracts

Review Methodology: Research questions were raised using PICO (population, intervention, comparison, and outcomes) and then validated to ensure that they had not been addressed by any other publications. In this case, P-desert locust, I-Bio-control, C-use of chemical pesticides, and O-success of application. A systematic review was then carried out using various keywords. The following search engines and databases were used: Google, Google Scholar, PubMed, ScienceDirect, FAO Desert Locust Information Service, CABI, and HINARI. Titles and abstracts were screened followed by full-text downloading and analysis. Some authors were contacted for full publications where only the abstracts were available.

Introduction which is approximately 20% of the earth’s surface [3]. In 1 day, the swarm is capable of consuming the same amount Desert locust (Schistocerca gregaria Forskål) is one of the of as approximately 35,000 people, with each locust most serious agricultural pests in the world due to its consuming about its own weight of green vegetation [4]. voracity, speed of reproduction, and range of flights, which The plagues are associated with great economic losses can cause huge damage to all plant species [1]. A single hence require urgent attention to safeguard livelihoods swarm can comprise of up to 80 million per square and the environment. kilometer and can more than 100 km in the direction of Desert locust invasion is usually restricted to the semi- prevailing winds to cover an area of about 1200 square arid and arid of that receives less than kilometers per day [2]. If left uncontrolled, desert locust 200 mm of rainfall annually [5]. In 1986–1989, desert locust can invade a total area of 28 million square kilometers, plague affected 43 countries after heavy rains. This plague

http://www.cabi.org/cabreviews 2 CAB Reviews ended mainly because of control operations and unusual vegetation [16]. If these conditions are unfavorable, the winds that blew swarms across the [6]. swarm migrates until it encounters favorable breeding A similar swarm was witnessed from 2003 to 2005 conditions, which may be thousands of kilometers away where more than 20 countries suffered with an estimated [12]. Effective preventive management strategy should 80–100% loss of crops especially in sub-Saharan Africa [7]. therefore not only rely on the knowledge of the pest During this time, control operations treated nearly biology and ecology but also on the environmental factors 130,000 per square kilometers of the locust infestation associated with its spread. area. The operation took 2 years and spent more than US$ Repeated outbreaks of desert locust in Africa have 400 million to end the plague [6]. Between 2019 and 2020, prompted the use of chemical pesticides as the main exceptional locust breeding was observed in the horn of preventive and control measures. Most of the locust Africa [4]. This magnitude of invasion had not been control measures carried out over the years have used witnessed for more than 70 years in East Africa. A conventional chemical (organochlorines, prediction model demonstrated that vast areas of Kenya, , , and ) that are northeastern regions of Uganda, and some regions of usually neurotoxic to the locust [17]. Although chemical Southern were at high risk of providing a breeding pesticides may provide an effective means of control due environment for the locust [8]. The onset of long rains to prolonged activity of the spray residue, increased season in East Africa would also remarkably increase the attention has been raised concerning environmental swarms, threatening and livelihoods [4]. This damage and human safety [18]. After treatment with rapid and sudden upsurge could be attributed to erratic chemicals, death of occurs within hours, making it climatic behavior that is triggered by global warming [9]. difficult to monitor the effects of spray applications However, predictions are mainly based on ecological especially for highly mobile species [19]. As an upsurge aspects but should also integrate the social, economic, and starts, only a few locusts are aggregated into treatable cultural aspects for effective control measures. targets and hence spraying leaves out many individuals that Desert locust is able to change its behavior and continue the upsurge and become aggregated at high physiology in response to environmental conditions, densities [13]. Some chemical insecticides have been transforming the swarms from harmless solitary insects to effective at preventing desert locust outbreaks at very destructive cohesive ones [10]. This feature allows locusts early stages of invasion under Saharan condition but they to survive some of the harshest environmental conditions simultaneously induce heavy mortality in some non-target on earth. Seasonal migration of the desert locust is groups [20]. Besides, the outbreaks occur in influenced by various factors such as rainfall, temperature, environmentally sensitive areas especially wetlands, near wind, and vegetation [11]. Favorable conditions for human settlements and to some extent in the protected breeding are moist soils to depths of 10–15 cm, moist bare areas with numerous migratory [21]. In East Africa, areas for egg-laying, and green vegetation for hopper current management strategy for desert locust swarms is development [12]. Sparse and erratic seasonal rains aerial spraying with chemical pesticides, which has affected support phase change from their solitary lifestyle to a humans, livestock, and the environment [8]. The concern group lifestyle (gregarious phase) that develop into an regarding use of chemical pesticides provides impetus for upsurge and eventually into a plague [13]. These density- investment in alternative means of control that are dependent changes are adaptations for migration under environmentally friendly and sustainable, such as bio- heterogeneous environmental conditions. For instance, a pesticides [13, 22] even though much remains to be done research study estimated the density of gregarization of in terms of research and implementation. desert locust hoppers in vegetation and reported that Successful control of desert locust will require the vegetation cover and height were the only characteristics development of an integrated pest management program that could enhance prediction of locust phase status [14]. using a variety of products that can be applied with a range A related study reported that low cover and dry vegetation of techniques that are appropriate in different habitats and led to a low density of gregarization while dense and green circumstances [23]. This must be associated with reduced vegetation favored a high density of gregarization, probably , economic costs, environmental risks, due to a dispersion rate of the individuals. Another and duration and extent of the locust threat [24]. Proposed experiment explored the influence of vegetation patterns products include bio-pesticides from plants and on gregarization and showed that when the distribution of microorganisms. They are recommended because of their the vegetation was patchy, the locusts were more active, high specificity, very little adverse impact on the experienced higher levels of crowding and became more environment, and are non-toxic to humans and livestock gregarious [15]. This demonstrates that vegetation when used at recommended doses [25]. A simulation distribution influences individual behavior and phase state model suggested that applying even a conservative rate of and plays a major role in population level responses. In a control from the beginning of an upsurge as part of early survey for early detection and control of desert locust in intervention would further reduce the size of upsurges Sudan, locust densities varied according to the amount and and plagues and would contribute to better management distribution of rainfall and longevity of the annual green of desert locust populations [23].

http://www.cabi.org/cabreviews Eunice W. Githae and Erick K. Kuria 3 Use of microorganisms as bio-control agents on the 6th day after treatment [34]. When M. flavoviride oil formulation was tested in the field, the treated locusts Only a few fungal and bacterial pathogens have been showed a reduction of hopper bands into small groups reported to show their efficacy against the desert locust with maximal daily mortality at 10–11 days in the open (Table 1). Entomopathogenic fungi are potentially the most field and 6–10 days in cages 19[ ]. A similar study in the field versatile bio-control agents due to their wide host range showed a population reduction of adult locusts by 90% in and natural occurrence, which makes them less damaging 10 days after application. In dense vegetation, the to the environment [42]. They are also slower acting than formulation resulted in 70% control within 14 days after chemicals thus best suitable during early infestations. application [35]. However, a major concern with an oil Entomopathogenic fungi and nematodes can be more formulation of M. flavoviride is its effects on non-target effective when applied on the soil surface rather than spray organisms especially bees [44], and therefore, safety testing treatment [38]. on such non-target organisms should be considered. Early research on the use of fungi as a bio-control agent Various publications have focused on the use of against desert locust was focused on . M. anisopliae as a bio-control The fungus was tested in both laboratory and field agent against many species [45]. Metarhizium anisopliae var. conditions and showed significant results. Treatments were acridum, commonly known as Metarhizium acridum in made using oil formulations that improved the efficacy as modern science [46], is an environmentally safer compared to water-based formulations. For example, commercial bio-pesticide that has been developed for ultra formulations of M. flavoviride in cottonseed oil showed low volume spraying [13]. The bio-pesticide kills about superior performance to water-based suspensions at low 70–90% of treated locusts within 14–20 days with no humidity hence applicability in less humid environments measurable impact on non-target organisms [47]. The [43]. In a laboratory experiment, adult desert locusts fungus produces destruxins in mycosed insects that kills inoculated with M. flavoviride reduced their daily food locusts even before the fungus has established itself. consumption and died within a period of 5–14 days [33]. Furthermore, the pathogen is unable to compete effectively The results concur with those reported on significant with the saprophytic flora and hence fails to sporulate 13[ ]. reduction in flight activity and food consumption on the Various laboratory and field trials have demonstrated the 3rd day after application, with a 100% mortality occurring efficacy ofM. anisopliae var. acridum on desert locust

Table 1. Species of microorganisms studied as bio-control agents against desert locust. No. Effect on desert locust Reference 1. Metarhizium anisopliae var. acridum Increased acidic phosphatase (AcP) for autophagy and [26] Driver & Milner defense Altered behavioral changes [27] Changed biochemistry and antimicrobial defenses [28] Less energy reserves and poor flight capability [29] 2. Metarhizium anisopliae var. acridum + Reduced feeding and mobility [30] Phenyl Aceto Nitrile (PAN) 3. Metarhizium anisopliae var. acridum + Mortality happened sooner than those infected with only [31] Paranosema (Nosema) locustae one of the pathogens (Protozoa) 4. Metarhizium anisopliae var. acridum + Significant reduction in total proteins and hemocyte counts [32] (Bals-Criv) Vuill. 5. Metarhizium flavoviride Gams & Rozsypal Reduction dispersal of hopper bands into small groups [19] Reduced daily food consumption [33] Significant reductions in flight activity and food [34] consumption High mortality in sparse vegetation than in dense [35] vegetation 6. Metarhizium robertsii J.F. Bisch., Produced Destruxin A which inhibited fever [36] S.A. Rehner & Humber 7. Serratia marcescens Bizio (Bacteria) Induced fever [37] 8. Beauveria bassiana, Entomophthora, and High mortality rates, although the nematode was more [38] Steinernema carpocapsae (Nematode) effective than fungi in less time 9. Bacillus weihenstephanensis and Showed the highest insecticidal activities against desert [39] Pseudomonas sp. (Bacteria) locust nymphs 10. Pseudomonas aeruginosa (Schroeter) Pathogenic bacterium of the desert locust [40] Migula (Bacteria) 11. Bacillus cereus (Bacteria) High insecticidal activity [41]

http://www.cabi.org/cabreviews 4 CAB Reviews although the results are highly variable. For example, desert locust fevered when infected with Serratia treatment of desert locust with the fungi increased acidic marcescens and this “behavioral fever” greatly delays the phosphatase (AcP) (a lysosomal enzyme that plays a role in progress of mycosis [37]. Other bacterial pathogens autophagy, cell turn over and defense) activity on day three isolated from the gut contents of desert locust, which after inoculation with the fungus. This was accompanied by showed the highest insecticidal activities against the locust a decline in the total hemocyte, plasmatocytes, and nymphs were Bacillus weihenstephanensis, Pseudomonas sp., coagulocytes [26]. However, desert locusts usually undergo Pseudomonas aeruginosa, and Bacillus cereus [39–41]. These thermoregulation (behavioral fever) during an infection to strains could be potential bio-control agents in controlling improve their immune system [37], although this declines desert locust nymphs. after continuous application. A laboratory study examined A workshop held in in 2007 on the future of the effects of fungus on survival and reproduction in adult bio-pesticides in desert locust management made various desert locust under various temperature conditions [27]. recommendations to ensure rapid integration of bio- Mortality rates were varied upon thermal conditions pesticides into operational desert locust management where it was more that 90% at 10 days after treatment [49]. However, much remains to be implemented with under constant temperature and 66% at 70 days after various shortcomings associated with the use of treatment under thermoregulatory conditions. Topical Metarhizium in desert locust control. The following are the application of M. anisopliae var acridum on the desert locust main ones: resulted in changes in the biochemistry and antimicrobial i. They are highly susceptible to the damaging effects of defenses of the from the second day post solar radiation [50] keeping in mind that desert locust application [28]. The fungus stimulated the hemolytic mostly invades areas that have harsh climatic aggregation indicating an overall stimulation of the immune conditions. To enhance survival, spores can be coated system, which declined by day four of application. A similar with water-soluble materials (anti-UV) that protect study assessed the effect of M. anisopliae var acridum on toxins and spores from solar radiation [50]. energy reserves and flight capability in desert locust and ii. Performance of the fungus may be affected by found a decline in carbohydrate and lipids in the hemolymph environmental factors such as humidity and 3 days after inoculation [29]. This indicates that the poor temperature [51, 52]. flight capability of mycosed locusts is partly due to a iii. Metarhizium has a narrow host range (only locusts and reduction in energy reserves. However, desert locusts ) as compared to chemical pesticides reared under crowded conditions are significantly more hence more expensive in terms of research, resistant to the fungi that solitary locusts due to elevated development, and registration costs [53]. antimicrobial activity at the gregarious phase [48]. These iv. Use of mycopesticides may have a possibility of causing behavioral changes may enable the locust to adapt to new health effects to immune-compromised persons environments hence the need for further research on the exposed to high doses through production and use [54]. use, testing and monitoring of the formulations. v. They are slower acting than chemical pesticides and The performance of M. anisopliae var. acridum against thus inappropriate for emergency situation [18], desert locust can be improved by combining the fungus though they may have a major role in an integrated with other bio-controls. For instance, when the fungus was control strategy. combined with the pheromone Phenyl Aceto Nitrile vi. Sporulation of the fungus takes a long period of time (PAN), the solution caused a 100% mortality of desert and requires conditions that are not always found in locust within 2 weeks and this could reduce cost and the field 55[ ]. environmental hazards [30]. Another study combined the fungus with microsporidian Paranosema (Nosema) locustae and showed that locust nymphs treated with both Use of botanical extracts as bio-control agents pathogens died more quickly than those infected with only one of the pathogens [31]. However, this study concluded Several studies have reported the use of botanical extracts that application of M. anisopliae might diminish the natural as potential bio-pesticides against desert locust. In this persistence of P. locustae. On the other hand, the combined review, a total of 27 plant species belonging to 20 families effect of M. anisopliae with Beauveria bassiana achieved a were identified as tested against desert locust (Table 2) significant reduction in total proteins and hemocyte counts but had varied results. Azadirachta indica and Melia volkensii of the desert locust on the 9th day of application [32]. were the most studied plant species, both belonging to Although these results indicate that a combination of Family Meliaceae, which is known to have biologically effective microorganisms may be useful while considering active limonoids [56]. These were followed by Calotropis integrated pest management strategy of the desert locust, procera, Fagonia bruguieri, and Peganum harmala. The most more research is necessary to assess the interactions of represented plant family was Apiaceae with a frequency of these microorganisms. 21%. However, most of these studies used crude extracts Several studies have shown the potential of bacteria as a and the active ingredients against desert locust were not bio-control agent against the desert locust. For example, identified.

http://www.cabi.org/cabreviews Eunice W. Githae and Erick K. Kuria 5 Table 2. List of plant species that have been tested as bio-control agents for desert locust. No. Scientific name Common name Family Frequency (%) 1. Azadirachta indica (A. Juss.) Brandis Neem Meliaceae 16.40 (10) 2. Melia volkensii Giirke Melia Meliaceae 11.48 (7) 3. Calotropis procera (Aiton) W.T. Aiton Sodom apple Apocynaceae 6.56 (4) 4. Fagonia bruguieri D.C Fagonia Zygophyllaceae 6.56 (4) 5. Peganum harmala L. Wild rue Nitrariaceae 6.56 (4) 6. Nerium oleander L. Oleander Apocynaceae 5.00 (3) 7. Allium cepa L. Onion Amaryllidaceae 3.28 (2) 8. Petroselinum sativum Hoffm. Parsley Apiaceae 3.28 (2) 9. Cuminum cyminum L. Cumin Apicaceae 3.28 (2) 10. Schouwia purpurea (Forssk.) Schweinf. Saharan crucifer Brassicaceae 3.28 (2) 11. Jatropha curcas L. Physic nut Euphorbiaceae 3.28 (2) 12. Ocimum basilicum L. Basil Lamiaceae 3.28 (2) 13. Nigella sativa L. Black seed/cumin Ranunculaceae 3.28 (2) 14. Zygophyllum gaetulum (Emb. & Maire) Caper beans Zygophyllaceae 3.28 (2) 15. Ammi visnaga (L.) Lam Toothpick weed Apiaceae 1.64 (1) 16. Solenostemma argel (Delile) Hayne Argel Asclepiadaceae 1.64 (1) 17. Matricaria chamomilla L. Chamomile Asteraceae 1.64 (1) 18. Cleome arabica L. The stinker Capparidaceae 1.64 (1) 19. Pelargonium radens H.E. Moore Radula Geraniaceae 1.64 (1) 20. Origanum vulgare L. Oregano Lamiaceae 1.64 (1) 21. Linum usitatissimum L. Flax, linseed Linaceae 1.64 (1) 22. Eucalyptus L’Hérit spp. Myrtle Myrtaceae 1.64 (1) 23. Zizyphus lotus (L.) Desf. Jujube Rhamnaceae 1.64 (1) 24. Rhizophora mucronata Lam. Mangrove Rhizophoraceae 1.64 (1) 25. Carum carvi L. Caraway Apiaceae 1.64 (1) 26. Citrus aurantium L. Orange Rutaceae 1.64 (1) 27. Gaultheria procumbens L. Wintergreen Ericaceae 1.64 (1)

Plant alkaloids have been reported to affect desert on the effect of C. procera, Schouwia purpurea, and Zizyphus locust in different ways. For instance, from lotus alkaloids on the desert locust observed morphological A. indica has an anti-feeding activity that inhibits feeding and changes, molting inhibition and anti-feeding effects with a molting [57]. The alkaloid has been formulated to produce significant mortality ranging from 45% to 53% on day five a commercial anti-feeding product that controls a wide after treatments [66]. In a different experiment, fruit range of plant pests without harming beneficial insects extracts of Ammi visnaga promoted the acidic phosphatase [58]. Anti-feeding activity of A. indica against desert locust (AcP) activity and reduced alkaline phosphatase (AlP) has also been well studied [58–60]. The activity varied in activity in fat bodies of adult desert locust. This was A. indica (79.62%), Jatropha curcas (78.92%), and Solenoste­ attributed to presence of couramins and furocoumarins mma argel (56%) against the desert locust with a significant [67]. Extracts of Fagonia bruguieri also inhibited growth and mortality of 43.39%, 40.54%, and 20.70%, respectively, after development of Desert locust by intervening with the 7 days of treatment. Further, cold-pressed A. indica seed oil process of metamorphosis [68, 69]. Meanwhile, desert resulted in molting disturbances and morphogenetic locust nymphs treated with Nerium oleander leave extracts defects of the wings, legs, and antennae [61]. When Nigella could not molt, had reduced food intake, and had a sativa extracts were compared with those of A. indica, cumulative mortality rate greater than 50% from the fourth N. sativa caused a decrease in the body weight but with no day of application and 100% mortality at the 12th day of mortality [58]. The effects of Calotropis procera, Zygophyllum application [70]. Extracts derived from different parts of gaetulum, and Peganum harmala on survival, feeding, and the Rhizophora mucronata have insecticidal and antifeedant reproduction in desert locust showed that all the alkaloids activity against the locust [71]. Melia volkensii extracts also extracted from the plants reduced food intake, increased have a growth inhibiting anti-feeding properties against weight loss, and caused a significant mortality 62[ ]. Alkaloids desert locust and other insect pests [72]. Field tests have extracted from C. procera and Z. gaetulum prevented sexual shown that the crude powder of M. volkensii has effective maturity both in males and female while those of P. harmala control resulting from acute toxicity, retarded growth, and reduced female fecundity and hatching rate. Both C. procera 80% malformations, which led to 100% mortality after and P. harmala generated 100% mortality within a few days 14 days [56, 73]. These botanicals have shown their after treatment and portrayed symptoms similar to those potential as bio-pesticides but are still at the experimental of insects treated with insecticides [63–65]. A similar study stage as far as desert locust control is concerned.

http://www.cabi.org/cabreviews 6 CAB Reviews Several studies have confirmed that essential oils are 3. Chen Y. Watch out for the outbreaks of desert locusts. effective against desert locusts and could be used as Entomological Knowledge 2002;39:335–9. natural controls. A novel mixture of plant oils that had 4. FAO. FAO and partners stress urgent need on Desert Locust high toxic effects on desert locust after a single spray Response. Building national and regional capacities for treatment was developed [55]. It was a combination of sustainable plant ; 2020. Available from: URL: three essential oils of Carum carvi, Citrus aurantium dulcis, www.fao.org and Gaultheria procumbens. Interestingly, a mean mortality 5. FAO. Desert Locust outbreak in Kenya. Available from: URL: rate of 80% was observed within 24 h after treatment. http://www.fao.org/emergencies/resources/photos/photo- detail/en/c/1258345/2020 Furthermore, essential oils extracted from 10 different plant species were tested against desert locust by topical 6. WMO, FAO. Weather and Desert Locusts; 2016; WMO-No. 1175 application [74]. Oil from Allium cepa proved to be the 7. Latchininsky A, Piou C, Franc A, Soti V. Applications of remote most toxic to the locusts followed by Petroselinum sensing to locust management. In: : Baghdadi N, Zribi M, sativum. Other plants studied were Pelargonium radula, editors. Land surface remote sensing. Elsevier, , UK: 2016. p. 263–93. Cuminum cyminum, Ocimum basilicum, Origanum vulgare, and Matricaria chamomilla, which showed different effects 8. Kimathi E, Tonnang HE, Subramanian S, Cressman K, against the locust. Combining the oils resulted in different Abdel-Rahman EM, Tesfayohannes M, et al. 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